{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T18:58:18Z","timestamp":1791917898469,"version":"4.3.4"},"reference-count":84,"publisher":"Ovid Technologies (Wolters Kluwer Health)","issue":"4","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JASN"],"published-print":{"date-parts":[[2018,4]]},"abstract":"<jats:p>\n                    Nonobstructive hydronephrosis, defined as dilatation of the renal pelvis with or without dilatation of the ureter, is the most common antenatal abnormality detected by fetal ultrasound. Yet, the etiology of nonobstructive hydronephrosis is poorly defined. We previously demonstrated that defective development of urinary tract pacemaker cells (utPMCs) expressing hyperpolarization-activated cyclic nucleotide-gated channel 3 (HCN3) and the stem cell marker cKIT causes abnormal ureteric peristalsis and nonobstructive hydronephrosis. However, further investigation of utPMC development and function is limited by lack of knowledge regarding the embryonic derivation, development, and molecular apparatus of these cells. Here, we used lineage tracing in mice to identify cells that give rise to utPMCs. Neural crest cells (NCCs) indelibly labeled with tdTomato expressed HCN3 and cKIT. Furthermore, purified HCN3+ and cKIT+ utPMCs were enriched in\n                    <jats:italic toggle=\"yes\">Sox10<\/jats:italic>\n                    and\n                    <jats:italic toggle=\"yes\">Tfap-2\u03b1<\/jats:italic>\n                    , markers of NCCs. Sequencing of purified RNA from HCN3+ cells revealed enrichment of a small subset of RNAs, including RNA encoding protein kinase 2\n                    <jats:italic toggle=\"yes\">\u03b2<\/jats:italic>\n                    (PTK2\n                    <jats:italic toggle=\"yes\">\u03b2<\/jats:italic>\n                    ), a Ca\n                    <jats:sup>2+<\/jats:sup>\n                    -dependent tyrosine kinase that regulates ion channel activity in neurons. Immunofluorescence analysis\n                    <jats:italic toggle=\"yes\">in situ<\/jats:italic>\n                    revealed PTK2\n                    <jats:italic toggle=\"yes\">\u03b2<\/jats:italic>\n                    expression in NCCs as early as embryonic day 12.5 and in HCN3+ and cKIT+ utPMCs as early as embryonic day 15.5, with sustained expression in HCN3+ utPMCs until postnatal week 8. Pharmacologic inhibition of PTK2\n                    <jats:italic toggle=\"yes\">\u03b2<\/jats:italic>\n                    in murine pyeloureteral tissue explants inhibited contraction frequency. Together, these results demonstrate that utPMCs are derived from NCCs, identify new markers of utPMCs, and demonstrate a functional contribution of PTK2\n                    <jats:italic toggle=\"yes\">\u03b2<\/jats:italic>\n                    to utPMC function.\n                  <\/jats:p>","DOI":"10.1681\/asn.2017090951","type":"journal-article","created":{"date-parts":[[2018,2,7]],"date-time":"2018-02-07T09:25:09Z","timestamp":1517995509000},"page":"1198-1209","source":"Crossref","is-referenced-by-count":14,"title":["Protein Kinase 2\u03b2 Is Expressed in Neural Crest-Derived Urinary Pacemaker Cells and Required for Pyeloureteric Contraction"],"prefix":"10.1681","volume":"29","author":[{"given":"Samir M.","family":"Iskander","sequence":"first","affiliation":[{"name":"Program in Developmental and Stem Cell Biology and"},{"name":"Departments of Laboratory Medicine and Pathobiology and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meghan M.","family":"Feeney","sequence":"additional","affiliation":[{"name":"Program in Developmental and Stem Cell Biology and"},{"name":"Departments of Laboratory Medicine and Pathobiology and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kirby","family":"Yee","sequence":"additional","affiliation":[{"name":"Program in Developmental and Stem Cell Biology and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Norman D.","family":"Rosenblum","sequence":"additional","affiliation":[{"name":"Program in Developmental and Stem Cell Biology and"},{"name":"Division of Nephrology, The Hospital for Sick Children, Toronto, Ontario, Canada; and"},{"name":"Departments of Laboratory Medicine and Pathobiology and"},{"name":"Paediatrics, University of Toronto, Toronto, Ontario, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"276","published-online":{"date-parts":[[2018,2,7]]},"reference":[{"key":"B1-20231016","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1113\/eph8702290","article-title":"Pyeloureteral motility and ureteral peristalsis: Essential role of sensory nerves and endogenous prostaglandins.","volume":"87","author":"Lang","year":"2002","journal-title":"Exp Physiol"},{"key":"B2-20231016","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1007\/s00467-013-2631-4","article-title":"Urinary tract pacemaker cells: Current knowledge and insights from nonrenal pacemaker cells provide a basis for future discovery.","volume":"29","author":"Feeney","year":"2014","journal-title":"Pediatr Nephrol"},{"key":"B3-20231016","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1097\/01.ju.0000141594.99139.3d","article-title":"c-kit and ureteral peristalsis.","volume":"173","author":"David","year":"2005","journal-title":"J Urol"},{"key":"B4-20231016","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1038\/ki.2009.483","article-title":"The pelvis-kidney junction contains HCN3, a hyperpolarization-activated cation channel that triggers ureter peristalsis.","volume":"77","author":"Hurtado","year":"2010","journal-title":"Kidney Int"},{"key":"B5-20231016","doi-asserted-by":"crossref","first-page":"730","DOI":"10.1096\/fj.13-237289","article-title":"A molecular signature of tissues with pacemaker activity in the heart and upper urinary tract involves coexpressed hyperpolarization-activated cation and T-type Ca2+ channels.","volume":"28","author":"Hurtado","year":"2014","journal-title":"FASEB J"},{"key":"B6-20231016","doi-asserted-by":"crossref","first-page":"F925","DOI":"10.1152\/ajprenal.00138.2002","article-title":"Identification of c-kit-positive cells in the mouse ureter: The interstitial cells of Cajal of the urinary tract.","volume":"284","author":"Pezzone","year":"2003","journal-title":"Am J 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and adrenergic activity in distal ureter of rabbits.","volume":"48","author":"Yalcin","year":"2013","journal-title":"J Pediatr Surg"},{"issue":"6 Pt B","key":"B33-20231016","doi-asserted-by":"crossref","first-page":"1028","DOI":"10.1016\/j.jpurol.2013.02.003","article-title":"Altered expression of interstitial cells of Cajal in primary obstructive megaureter.","volume":"9","author":"Kart","year":"2013","journal-title":"J Pediatr Urol"},{"key":"B34-20231016","doi-asserted-by":"crossref","first-page":"412","DOI":"10.7150\/ijms.14880","article-title":"The expression of Gli3 and Teashirt3 in the stenotic tissue of congenital pelvi-ureteric junction obstruction in children.","volume":"13","author":"Chen","year":"2016","journal-title":"Int J Med Sci"},{"key":"B35-20231016","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1242\/dev.113.3.723","article-title":"Developmental analysis of the retinoic acid-inducible RAR-beta 2 promoter in transgenic 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